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Current Evidence for a Paradigm Shift in Gastric Cancer Prevention From Endoscopic Screening to Helicobacter pylori Eradication in Korea

  • Kim, Young-Il (Center for Gastric Cancer, National Cancer Center) ;
  • Choi, Il Ju (Center for Gastric Cancer, National Cancer Center)
  • Received : 2022.07.04
  • Accepted : 2022.07.25
  • Published : 2022.07.31

Abstract

Gastric cancer is prevalent in Korea and ranked as the third most common cancer in 2019, followed by lung and thyroid cancers. The National Cancer Screening Program (NCSP) for gastric cancer has been implemented in adults aged ≥ 40 since 1999 and involves endoscopic screening every 2 years. The beneficial effects of the current NCSP on early cancer detection, cost-effectiveness, and mortality reduction are evident. However, the screening program results in a large socioeconomic burden and the consumption of medical resources, as it focuses solely on secondary prevention (early detection) rather than primary prevention of cancer. Helicobacter pylori is defined as a group I carcinogen by the International Agency for Research on Cancer. Hence, its eradication has been suggested as an important primary gastric cancer prevention strategy. Well-designed randomized controlled trials involving high-risk groups (post-endoscopic resection of early gastric cancer and family history of gastric cancer) and long-term follow-up studies in the general population have provided high-quality evidence regarding the effects of H. pylori eradication on gastric cancer prevention. In this review, we discussed the evidences for a possible modification of the current gastric cancer secondary prevention strategy by introducing primary prevention through H. pylori eradication. Areas for future research to optimize primary prevention strategies were also suggested.

Keywords

Acknowledgement

This work was supported by grants from the National Cancer Center (grant numbers: NCC 2210630-1).

References

  1. Kang MJ, Won YJ, Lee JJ, Jung KW, Kim HJ, Kong HJ, et al. Cancer statistics in Korea: incidence, mortality, survival, and prevalence in 2019. Cancer Res Treat 2022;54:330-344. https://doi.org/10.4143/crt.2022.128
  2. Hong S, Won YJ, Lee JJ, Jung KW, Kong HJ, Im JS, et al. Cancer statistics in Korea: incidence, mortality, survival, and prevalence in 2018. Cancer Res Treat 2021;53:301-315. https://doi.org/10.4143/crt.2021.291
  3. Kim Y, Jun JK, Choi KS, Lee HY, Park EC. Overview of the National Cancer screening programme and the cancer screening status in Korea. Asian Pac J Cancer Prev 2011;12:725-730. PUBMED
  4. Park HA, Lee SK, Kim SG, Shim KN, Park SM, Lee SY, et al. The Korean guideline for gastric cancer screening. J Korean Med Assoc 2015;58:373-384. https://doi.org/10.5124/jkma.2015.58.5.373
  5. Choi KS, Jun JK, Suh M, Park B, Noh DK, Song SH, et al. Effect of endoscopy screening on stage at gastric cancer diagnosis: results of the National Cancer Screening Programme in Korea. Br J Cancer 2015;112:608-612. https://doi.org/10.1038/bjc.2014.608
  6. Jun JK, Choi KS, Lee HY, Suh M, Park B, Song SH, et al. Effectiveness of the Korean National Cancer Screening Program in reducing gastric cancer mortality. Gastroenterology 2017;152:1319-1328.e7. https://doi.org/10.1053/j.gastro.2017.01.029
  7. Korea Central Cancer Registry. Annual report of cancer statistics in Korea in 2019 [Internet]. Goyang: Korea Central Cancer Registry; 2021 [cited 2022 Jun 11]. Available from: https://ncc.re.kr/ cancerStatsView.ncc?bbsnum=578&searchKey=total&searchValue=&pageNum=1.
  8. Lee S, Jun JK, Suh M, Park B, Noh DK, Jung KW, et al. Gastric cancer screening uptake trends in Korea: results for the National Cancer Screening Program from 2002 to 2011: a prospective cross-sectional study. Medicine (Baltimore) 2015;94:e533. https://doi.org/10.1097/MD.0000000000000533
  9. Korean Statistical Information Service. National health screening statistics [Internet]. Daejeon: Statistics Korea; 2021 [cited 2022 Jun 12]. Available from: https://kosis.kr/statisticsList/statisticsListIndex.do?menuId=M_01_01&vwcd=MT_ZTITLE&parmTabId=M_01_01&parentId=F.1;F_8.2;&outLink=Y#F_8.2.
  10. Hong S, Lee YY, Lee J, Kim Y, Choi KS, Jun JK, et al. Trends in cancer screening rates among Korean men and women: results of the Korean National Cancer Screening Survey, 2004-2018. Cancer Res Treat 2021;53:330-338. https://doi.org/10.4143/crt.2020.263
  11. Lee W. Application of current image-enhanced endoscopy in gastric diseases. Clin Endosc 2021;54:477-487. https://doi.org/10.5946/ce.2021.160
  12. Takahashi H, Miura Y, Osawa H, Takezawa T, Ino Y, Okada M, et al. Blue laser imaging with a smallcaliber endoscope facilitates detection of early gastric cancer. Clin Endosc 2019;52:273-277. https://doi.org/10.5946/ce.2018.100
  13. Kim H, Hwang Y, Sung H, Jang J, Ahn C, Kim SG, et al. Effectiveness of gastric cancer screening on gastric cancer incidence and mortality in a community-based prospective cohort. Cancer Res Treat 2018;50:582-589. https://doi.org/10.4143/crt.2017.048
  14. Kim JH, Han KD, Lee JK, Kim HS, Cha JM, Park S, et al. Association between the National Cancer Screening Programme (NSCP) for gastric cancer and oesophageal cancer mortality. Br J Cancer 2020;123:480-486. https://doi.org/10.1038/s41416-020-0883-x
  15. Nam SY, Choi IJ, Park KW, Kim CG, Lee JY, Kook MC, et al. Effect of repeated endoscopic screening on the incidence and treatment of gastric cancer in health screenees. Eur J Gastroenterol Hepatol 2009;21:855-860. https://doi.org/10.1097/MEG.0b013e328318ed42
  16. Information Committee of the Korean Gastric Cancer Association. Korean Gastric Cancer Association-Led Nationwide Survey on Surgically Treated Gastric Cancers in 2019. J Gastric Cancer 2021;21:221-235. https://doi.org/10.5230/jgc.2021.21.e27
  17. Jung Y, Kim JW, Im JP, Cho YK, Lee TH, Jang JY. Safety of gastrointestinal endoscopy in Korea: a nationwide survey and population-based study. J Korean Med Sci 2022;37:e24. https://doi.org/10.3346/jkms.2022.37.e24
  18. Cheung DY, Jang BI, Kim SW, Kim JH, Kim HK, Shin JE, et al. Multidisciplinary and multisociety practice guideline on reprocessing flexible gastrointestinal endoscopes and endoscopic accessories. Clin Endosc 2020;53:276-285. https://doi.org/10.5946/ce.2020.106
  19. Choi SI, Park B, Joo J, Kim YI, Lee JY, Kim CG, et al. Three-year interval for endoscopic screening may reduce the mortality in patients with gastric cancer. Surg Endosc 2019;33:861-869. https://doi.org/10.1007/s00464-018-6353-3
  20. Park CH, Kim EH, Chung H, Lee H, Park JC, Shin SK, et al. The optimal endoscopic screening interval for detecting early gastric neoplasms. Gastrointest Endosc 2014;80:253-259. https://doi.org/10.1016/j.gie.2014.01.030
  21. Nam JH, Choi IJ, Cho SJ, Kim CG, Jun JK, Choi KS, et al. Association of the interval between endoscopies with gastric cancer stage at diagnosis in a region of high prevalence. Cancer 2012;118:4953-4960. https://doi.org/10.1002/cncr.27495
  22. Hamashima C. Cancer screening guidelines and policy making: 15 years of experience in cancer screening guideline development in Japan. Jpn J Clin Oncol 2018;48:278-286. https://doi.org/10.1093/jjco/hyx190
  23. Pimentel-Nunes P, Libanio D, Marcos-Pinto R, Areia M, Leja M, Esposito G, et al. Management of epithelial precancerous conditions and lesions in the stomach (MAPS II): European Society of Gastrointestinal Endoscopy (ESGE), European Helicobacter and Microbiota Study Group (EHMSG), European Society of Pathology (ESP), and Sociedade Portuguesa de Endoscopia Digestiva (SPED) guideline update 2019. Endoscopy 2019;51:365-388. https://doi.org/10.1055/a-0859-1883
  24. Banks M, Graham D, Jansen M, Gotoda T, Coda S, di Pietro M, et al. British Society of Gastroenterology guidelines on the diagnosis and management of patients at risk of gastric adenocarcinoma. Gut 2019;68:1545-1575. https://doi.org/10.1136/gutjnl-2018-318126
  25. Liou JM, Malfertheiner P, Lee YC, Sheu BS, Sugano K, Cheng HC, et al. Screening and eradication of Helicobacter pylori for gastric cancer prevention: the Taipei global consensus. Gut 2020;69:2093-2112. https://doi.org/10.1136/gutjnl-2020-322368
  26. Shah SC, Piazuelo MB, Kuipers EJ, Li D. AGA clinical practice update on the diagnosis and management of atrophic gastritis: expert review. Gastroenterology 2021;161:1325-1332.e7. https://doi.org/10.1053/j.gastro.2021.06.078
  27. Guideline Committee of the Korean Gastric Cancer Association (KGCA), Development Working Group & Review Panel. Korean Practice Guideline for Gastric Cancer 2018: an Evidence-based, Multi-disciplinary Approach. J Gastric Cancer 2019;19:1-48. https://doi.org/10.5230/jgc.2019.19.e8
  28. Japanese Gastric Cancer Association. Japanese gastric cancer treatment guidelines 2018 (5th edition). Gastric Cancer 2021;24:1-21. https://doi.org/10.1007/s10120-020-01042-y
  29. Mori G, Nakajima T, Asada K, Shimazu T, Yamamichi N, Maekita T, et al. Incidence of and risk factors for metachronous gastric cancer after endoscopic resection and successful Helicobacter pylori eradication: results of a large-scale, multicenter cohort study in Japan. Gastric Cancer 2016;19:911-918. https://doi.org/10.1007/s10120-015-0544-6
  30. Fukase K, Kato M, Kikuchi S, Inoue K, Uemura N, Okamoto S, et al. Effect of eradication of Helicobacter pylori on incidence of metachronous gastric carcinoma after endoscopic resection of early gastric cancer: an open-label, randomised controlled trial. Lancet 2008;372:392-397. https://doi.org/10.1016/S0140-6736(08)61159-9
  31. Choi J, Kim SG, Yoon H, Im JP, Kim JS, Kim WH, et al. Eradication of Helicobacter pylori after endoscopic resection of gastric tumors does not reduce incidence of metachronous gastric carcinoma. Clin Gastroenterol Hepatol 2014;12:793-800.e1. https://doi.org/10.1016/j.cgh.2013.09.057
  32. Choi JM, Kim SG, Choi J, Park JY, Oh S, Yang HJ, et al. Effects of Helicobacter pylori eradication for metachronous gastric cancer prevention: a randomized controlled trial. Gastrointest Endosc 2018;88:475-485.e2. https://doi.org/10.1016/j.gie.2018.05.009
  33. Choi IJ, Kook MC, Kim YI, Cho SJ, Lee JY, Kim CG, et al. Helicobacter pylori therapy for the prevention of metachronous gastric cancer. N Engl J Med 2018;378:1085-1095. https://doi.org/10.1056/NEJMoa1708423
  34. Ford AC, Yuan Y, Moayyedi P. Helicobacter pylori eradication therapy to prevent gastric cancer: systematic review and meta-analysis. Gut 2020;69:2113-2121. https://doi.org/10.1136/gutjnl-2020-320839
  35. Cho SJ, Choi IJ, Kook MC, Yoon H, Park S, Kim CG, et al. Randomised clinical trial: the effects of Helicobacter pylori eradication on glandular atrophy and intestinal metaplasia after subtotal gastrectomy for gastric cancer. Aliment Pharmacol Ther 2013;38:477-489. https://doi.org/10.1111/apt.12402
  36. Kim YI, Cho SJ, Lee JY, Kim CG, Kook MC, Ryu KW, et al. Effect of Helicobacter pylori eradication on long-term survival after distal gastrectomy for gastric cancer. Cancer Res Treat 2016;48:1020-1029. https://doi.org/10.4143/crt.2015.264
  37. Choi YJ, Kim N. Gastric cancer and family history. Korean J Intern Med 2016;31:1042-1053. https://doi.org/10.3904/kjim.2016.147
  38. Brenner H, Bode G, Boeing H. Helicobacter pylori infection among offspring of patients with stomach cancer. Gastroenterology 2000;118:31-35. https://doi.org/10.1016/S0016-5085(00)70411-2
  39. El-Omar EM, Oien K, Murray LS, El-Nujumi A, Wirz A, Gillen D, et al. Increased prevalence of precancerous changes in relatives of gastric cancer patients: critical role of H. pylori. Gastroenterology 2000;118:22-30. https://doi.org/10.1016/S0016-5085(00)70410-0
  40. Malfertheiner P, Megraud F, O'Morain CA, Gisbert JP, Kuipers EJ, Axon AT, et al. Management of Helicobacter pylori infection-the Maastricht V/Florence Consensus Report. Gut 2017;66:6-30. https://doi.org/10.1136/gutjnl-2016-312288
  41. Chey WD, Leontiadis GI, Howden CW, Moss SF. ACG clinical guideline: treatment of Helicobacter pylori infection. Am J Gastroenterol 2017;112:212-239. https://doi.org/10.1038/ajg.2016.563
  42. Choi IJ, Kim CG, Lee JY, Kim YI, Kook MC, Park B, et al. Family history of gastric cancer and Helicobacter pylori treatment. N Engl J Med 2020;382:427-436. https://doi.org/10.1056/NEJMoa1909666
  43. Chiang TH, Chang WJ, Chen SL, Yen AM, Fann JC, Chiu SY, et al. Mass eradication of Helicobacter pylori to reduce gastric cancer incidence and mortality: a long-term cohort study on Matsu Islands. Gut 2021;70:243-250. https://doi.org/10.1136/gutjnl-2020-322200
  44. Wong BC, Lam SK, Wong WM, Chen JS, Zheng TT, Feng RE, et al. Helicobacter pylori eradication to prevent gastric cancer in a high-risk region of China: a randomized controlled trial. JAMA 2004;291:187-194. https://doi.org/10.1001/jama.291.2.187
  45. Yan L, Chen Y, Chen F, Tao T, Hu Z, Wang J, et al. Effect of Helicobacter pylori eradication on gastric cancer prevention: updated report from a randomized controlled trial with 26.5 years of follow-up. Gastroenterology 2022;163:154-162.e3. https://doi.org/10.1053/j.gastro.2022.03.039
  46. You WC, Brown LM, Zhang L, Li JY, Jin ML, Chang YS, et al. Randomized double-blind factorial trial of three treatments to reduce the prevalence of precancerous gastric lesions. J Natl Cancer Inst 2006;98:974-983. https://doi.org/10.1093/jnci/djj264
  47. Li WQ, Zhang JY, Ma JL, Li ZX, Zhang L, Zhang Y, et al. Effects of Helicobacter pylori treatment and vitamin and garlic supplementation on gastric cancer incidence and mortality: follow-up of a randomized intervention trial. BMJ 2019;366:l5016.
  48. Pan KF, Zhang L, Gerhard M, Ma JL, Liu WD, Ulm K, et al. A large randomised controlled intervention trial to prevent gastric cancer by eradication of Helicobacter pylori in Linqu County, China: baseline results and factors affecting the eradication. Gut 2016;65:9-18. https://doi.org/10.1136/gutjnl-2015-309197
  49. ClinicalTrials.gov. Helicobacter pylori Eradication for Gastric Cancer Prevention in the General Population (HELPER) [Internet]. Bethesda (MD): U.S. National Library of Medicine; 2022 [cited 2022 Mar 14]. Available from: https://clinicaltrials.gov/ct2/show/NCT02112214?term=choi+il+ju&cntry=KR&draw=2&rank=8.
  50. Khan MY, Aslam A, Mihali AB, Shabbir Rawala M, Dirweesh A, Khan S, et al. Effectiveness of Helicobacter pylori eradication in preventing metachronous gastric cancer and preneoplastic lesions. A systematic review and meta-analysis. Eur J Gastroenterol Hepatol 2020;32:686-694.
  51. Chen HN, Wang Z, Li X, Zhou ZG. Helicobacter pylori eradication cannot reduce the risk of gastric cancer in patients with intestinal metaplasia and dysplasia: evidence from a meta-analysis. Gastric Cancer 2016;19:166-175. https://doi.org/10.1007/s10120-015-0462-7
  52. Rokkas T, Rokka A, Portincasa P. A systematic review and meta-analysis of the role of Helicobacter pylori eradication in preventing gastric cancer. Ann Gastroenterol 2017;30:414-423.
  53. Kim YJ, Chung WC. Is serum pepsinogen testing necessary in populationbased screening for gastric cancer? Korean J Intern Med 2020;35:544-546. https://doi.org/10.3904/kjim.2020.139
  54. Tong Y, Wang H, Zhao Y, He X, Xu H, Li H, et al. Serum pepsinogen levels in different regions of China and its influencing factors: a multicenter cross-sectional study. BMC Gastroenterol 2021;21:264. https://doi.org/10.1186/s12876-021-01794-6
  55. Quach DT, Hiyama T. Assessment of endoscopic gastric atrophy according to the Kimura-Takemoto classification and its potential application in daily practice. Clin Endosc 2019;52:321-327. https://doi.org/10.5946/ce.2019.072
  56. Miwata T, Quach DT, Hiyama T, Aoki R, Le HM, Tran PL, et al. Interobserver and intraobserver agreement for gastric mucosa atrophy. BMC Gastroenterol 2015;15:95. https://doi.org/10.1186/s12876-015-0327-x
  57. Jin EH, Chung SJ, Lim JH, Chung GE, Lee C, Yang JI, et al. Training effect on the inter-observer agreement in endoscopic diagnosis and grading of atrophic gastritis according to level of endoscopic experience. J Korean Med Sci 2018;33:e117. https://doi.org/10.3346/jkms.2018.33.e117
  58. Dixon MF, Genta RM, Yardley JH, Correa P. Classification and grading of gastritis. The updated Sydney System. International Workshop on the Histopathology of Gastritis, Houston 1994. Am J Surg Pathol 1996;20:1161-1181.
  59. Kim SS, Kook MC, Shin OR, Kim HS, Bae HI, Seo AN, et al. Factors to improve the interobserver agreement for gastric atrophy and intestinal metaplasia: consensus of definition and criteria. Histopathology 2018;72:838-845. https://doi.org/10.1111/his.13442
  60. Rugge M, Correa P, Di Mario F, El-Omar E, Fiocca R, Geboes K, et al. OLGA staging for gastritis: a tutorial. Dig Liver Dis 2008;40:650-658. https://doi.org/10.1016/j.dld.2008.02.030
  61. Capelle LG, de Vries AC, Haringsma J, Ter Borg F, de Vries RA, Bruno MJ, et al. The staging of gastritis with the OLGA system by using intestinal metaplasia as an accurate alternative for atrophic gastritis. Gastrointest Endosc 2010;71:1150-1158. https://doi.org/10.1016/j.gie.2009.12.029
  62. Cho SJ, Choi IJ, Kook MC, Nam BH, Kim CG, Lee JY, et al. Staging of intestinal- and diffuse-type gastric cancers with the OLGA and OLGIM staging systems. Aliment Pharmacol Ther 2013;38:1292-1302. https://doi.org/10.1111/apt.12515
  63. Nam JH, Choi IJ, Kook MC, Lee JY, Cho SJ, Nam SY, et al. OLGA and OLGIM stage distribution according to age and Helicobacter pylori status in the Korean population. Helicobacter 2014;19:81-89. https://doi.org/10.1111/hel.12112
  64. Rugge M, Meggio A, Pravadelli C, Barbareschi M, Fassan M, Gentilini M, et al. Gastritis staging in the endoscopic follow-up for the secondary prevention of gastric cancer: a 5-year prospective study of 1755 patients. Gut 2019;68:11-17. https://doi.org/10.1136/gutjnl-2017-314600
  65. Kwak HW, Choi IJ, Cho SJ, Lee JY, Kim CG, Kook MC, et al. Characteristics of gastric cancer according to Helicobacter pylori infection status. J Gastroenterol Hepatol 2014;29:1671-1677. https://doi.org/10.1111/jgh.12605
  66. Gyawali B, Kesselheim AS, D'Andrea E. Does Helicobacter pylori eradication therapy to prevent gastric cancer increase all-cause mortality? Int J Cancer 2019;144:411-412. https://doi.org/10.1002/ijc.31772